Polyembryonic Insects: An Extreme Clonal Reproductive Strategy (Entomology Monographs) 9811509573, 9789811509575

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Entomology Monographs

Kikuo Iwabuchi

Polyembryonic Insects An Extreme Clonal Reproductive Strategy

Entomology Monographs Series Editor Hideharu Numata, Graduate School of Science, Kyoto University, Sakyo-ku, Kyoto, Japan

Insects are the most diverse group of organisms, and many biological advances have been derived from this group. Although entomology is considered to be a classic science, recent developments in molecular methods, application of modern theoretical concepts and collaboration with related sciences have opened new directions in entomology. Japanese scientists play a significant role in these fields, and this book series will focus on such developments. The book series Entomology Monographs publishes refereed volumes on all aspects of entomology, including ecology, ethology, physiology, taxonomy, systematics, morphology, evolutionary developmental biology, genetics, biochemistry, and molecular biology in insects and related arthropods. Authors are not restricted to Japanese entomologists, and other international experts will also be considered on the basis of their recent contribution to these fields.

More information about this series at http://www.springer.com/series/15687

Kikuo Iwabuchi

Polyembryonic Insects An Extreme Clonal Reproductive Strategy

Kikuo Iwabuchi Tokyo University of Agriculture and Technology Fuchu, Tokyo, Japan

ISSN 2522-526X ISSN 2522-5278 (electronic) Entomology Monographs ISBN 978-981-15-0957-5 ISBN 978-981-15-0958-2 (eBook) https://doi.org/10.1007/978-981-15-0958-2 © Springer Nature Singapore Pte Ltd. 2019 This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors, and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, expressed or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. This Springer imprint is published by the registered company Springer Nature Singapore Pte Ltd. The registered company address is: 152 Beach Road, #21-01/04 Gateway East, Singapore 189721, Singapore

Preface

Polyembryony is a unique mode of reproduction in which many embryos are clonally produced from a single egg. In humans and animals, twins are occasionally produced from a single zygote. However, in some animal groups, polyembryony is found in normal reproduction and in some hymenopteran species, the number of offspring produced by polyembryony reaches more than 2000. Polyembryonic insects were first discovered in the late 1800s, and studies on polyembryony in encyrtids flourished in the early 1990s. Over the last several decades, the study of polyembryonic insects has advanced considerably. Many interesting results had been obtained since then. Nevertheless, the classical reports also continue to provide valuable knowledge that can be applied to current studies. Quite a few well-documented reviews have been published on the polyembryony of insects until today in each scientific discipline, e.g., ecology, physiology, and developmental biology (in situ, embryology). Thus, we still have no overall review of animal “polyembryology (i.e., biology of polyembryony).” Accordingly, finding the information of general biology of polyembryony is often very difficult for scientists outside of, or relatively new to, this field. Our most important question in polyembryonic insects is “how and why these species reproduce offspring clonally?” In addition, many biologically unique properties such as sterile larval castes and a novel mode of host invasion by morula-stage embryos are present. This book aims at integrating and summarizing the knowledge of all fields of polyembryony in insects (and some vertebrate animals), from cellular, developmental biological, physiological, molecular biological, sociobiological, and evolutionary biological viewpoints. It provides information about the mechanisms of polyembryogenesis, tissue-compatible invasion into the host which is the first case of compatible cellular interaction between phylogenetically distant organisms without rejection, the sex difference in defense, and the environmental regulation of caste structure. The book promotes the exciting potential of understanding the polyembryonic insects and the impact on life sciences.

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To my knowledge, a book devoted to the polyembryony in insects has never been published. There has been a book on the polyembryony of plants, but the polyembryony in plants differs from that in animals in terms of origin. There have also been books on the twins of humans; however, many efforts are focused on the social individuality and the genetics and epigenetics of identity. This book is for professional scientists in entomology, parasitology, ontogeny, reproductive biology, developmental biology, sociobiology, and evolutionary developmental biology (EvoDevo), and postgraduate students in these fields. The publication of this book would not be possible without the help of many persons. At first, I would like to give special thanks to the Series Editor, Prof. Dr. Hideharu Numata, from Kyoto University for giving me the opportunity to write this book and for his constant encouragement. I am extremely grateful to the staff at Springer, especially Ms. Fumiko Yamaguchi, Mr. Sivachandran Ravanan, and Ms. Camilya Anitta, for their patience. I wish to acknowledge the help and support given to us by my collaborators and colleagues. My thanks are directed to my co-workers, Prof. Dr. Jin Yoshimura, Dr. Hiroko Tabunoki, Mr. Takuma Sakamoto, and Ms. Maaya Nishiko, for reading the manuscript and drawing the figures. This work was supported by JSPS KAKENHI (15H02483). Tokyo, Japan

Kikuo Iwabuchi

Contents

1

Overview of Polyembryony . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.1 Definition of Polyembryony . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.2 Category of Polyembryony . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.3 Polyembryony in Animals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.3.1 Cnidaria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.3.2 Bryozoa (Ectoprocta) . . . . . . . . . . . . . . . . . . . . . . . . . . 1.3.3 Platyhelminthes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.3.4 Echinodermata . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.3.5 Chordata . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.3.6 Arthropoda, exclusive of Insecta . . . . . . . . . . . . . . . . . . 1.3.7 Insecta . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.4 Polyembryony in Hymenoptera, Exclusive of Encyrtidae . . . . . . . 1.4.1 Dryinidae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.4.2 Platygastridae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.4.3 Braconidae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1 1 2 3 4 5 7 8 10 13 14 23 23 24 29 36

2

Polyembryony in Encyrtid Parasitoids . . . . . . . . . . . . . . . . . . . . . . 2.1 List of Polyembryonic Species in Encyrtidae . . . . . . . . . . . . . . 2.1.1 Ageniaspis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1.2 Copidosoma . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2 Introduction to Polyembryony in the Genus Ageniaspis . . . . . . . 2.2.1 Ageniaspis atricollis . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.2 Ageniaspis bicoloripes . . . . . . . . . . . . . . . . . . . . . . . . 2.2.3 Ageniaspis citricola . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.4 Ageniaspis fuscicollis . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.5 Ageniaspis mayri . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.6 Ageniaspis testaceipes . . . . . . . . . . . . . . . . . . . . . . . . 2.3 Introduction to Polyembryony in the Genus Copidosoma . . . . . . 2.3.1 Copidosoma aithyia . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3.2 Copidosoma ancharus . . . . . . . . . . . . . . . . . . . . . . . .

45 45 45 47 53 53 54 54 55 56 56 57 57 57

. . . . . . . . . . . . . .

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2.3.3 Copidosoma aretas . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3.4 Copidosoma bakeri . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3.5 Copidosoma boucheanum . . . . . . . . . . . . . . . . . . . . . . . 2.3.6 Copidosoma desantisi . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3.7 Copidosoma filicorne . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3.8 Copidosoma floridanum . . . . . . . . . . . . . . . . . . . . . . . . 2.3.9 Copidosoma gelechiae . . . . . . . . . . . . . . . . . . . . . . . . . 2.3.10 Copidosoma koehleri . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3.11 Copidosoma peticus . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3.12 Copidosoma plethoricum . . . . . . . . . . . . . . . . . . . . . . . 2.3.13 Copidosoma sosares . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3.14 Copidosoma tanytmemus . . . . . . . . . . . . . . . . . . . . . . . 2.3.15 Copidosoma thompsoni . . . . . . . . . . . . . . . . . . . . . . . . 2.3.16 Copidosoma truncatellum . . . . . . . . . . . . . . . . . . . . . . . 2.3.17 Copidosoma varicorne . . . . . . . . . . . . . . . . . . . . . . . . . 2.4 Embryonic Development in Polyembryonic Encyrtidae . . . . . . . . 2.4.1 Classical Observations . . . . . . . . . . . . . . . . . . . . . . . . . 2.4.2 Current Knowledge on Early Embryonic Development in Copidosoma floridanum . . . . . . . . . . . . . . . . . . . . . . . . 2.4.3 Proliferation of Copidosoma floridanum Embryos . . . . . 2.4.4 Morphogenesis in Copidosoma floridanum Embryos . . . 2.4.5 Pattern Formation and Retainment of an Undifferentiated State in Copidosoma floridanum . . . . . . . . . . . . . . . . . . 2.4.6 Germ Cell Formation in Copidosoma floridanum . . . . . . 2.4.7 Does Copidosoma floridanum Have a Short or Long Germ Band? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4.8 Trophamnion/Extraembryonic Membrane of Polyembryonic Encyrtidae . . . . . . . . . . . . . . . . . . . . . . 2.4.9 Precocious Larvae of Copidosoma floridanum . . . . . . . . 2.4.10 Differences in Polyembryonic Development Between Encyrtidae and Braconidae . . . . . . . . . . . . . . . . . . . . . . 2.4.11 Comparison of Embryogenesis in Copidosoma floridanum and Mammals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4.12 Genomic Features of Polyembryony in Copidosoma floridanum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3

59 59 60 60 61 61 63 64 65 65 65 66 66 67 67 68 68 70 72 76 77 78 79 80 82 82 84 85 86

Host–Polyembryonic Parasitoid Interactions . . . . . . . . . . . . . . . . . . . 95 3.1 Evasion of the Host Immune System and Methods of Host Entry . . . 96 3.1.1 Overview of the Insect Immune System . . . . . . . . . . . . . 96 3.1.2 Parasitoid Resistance Mechanisms Against Host Immune Responses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 98 3.1.3 Passive Evasion of the Host Immune System by the Polyembryonic Braconid Macrocentrus cingulum . . . . . . 103

Contents

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3.1.4

Host Entry by Tissue-Compatible Invasion in the Polyembryonic Encyrtid Copidosoma floridanum . . . . . . 3.1.5 Enhancement of Host Immunity by Copidosoma floridanum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2 Physiological Interactions Between Parasitoids and Their Hosts . . . 3.2.1 Developmental Synchrony with the Host . . . . . . . . . . . . 3.2.2 Hormonal Regulation of Polyembryonic Development in Copidosoma floridanum . . . . . . . . . . . . . . . . . . . . . . 3.2.3 Effect of Host Condition on Survival and Brood Size . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4

Sociality in Polyembryonic Parasitoids . . . . . . . . . . . . . . . . . . . . . . . 4.1 Occurrence and Development of Precocious Larvae . . . . . . . . . . 4.1.1 Polyembryonic Species with Precocious Larvae . . . . . . . 4.1.2 Development of Precocious Larvae . . . . . . . . . . . . . . . . 4.2 Determination of Larval Morphs . . . . . . . . . . . . . . . . . . . . . . . . 4.3 Role of the Precocious Larvae as a Soldier Caste . . . . . . . . . . . . 4.3.1 Interspecific Competition Involving Copidosoma tanytmemus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3.2 Interspecific Competition Involving Copidosoma floridanum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3.3 Precocious Larvae as a Soldier Caste and Sex Differences in Aggressiveness in Copidosoma floridanum . . . . . . . . 4.3.4 Inter- and Intraspecific Competition in Copidosoma bakeri . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3.5 Intraspecific Competition in Copidosoma koehleri . . . . . 4.3.6 Inter- and Intraspecific Competition in Copidosoma desantisi . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3.7 Adaptive Increase in Precocious Larvae in Copidosoma floridanum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3.8 Environmental Effects on Soldier Production in Copidosoma floridanum . . . . . . . . . . . . . . . . . . . . . . . . 4.3.9 Presence of a Humoral Toxic Factor in Copidosoma floridanum . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.4 Sexual Conflict in Mixed-Sex Broods and Evolution of the Sterile Soldier Caste in Copidosoma floridanum . . . . . . . . . . . . . . . . . . 4.4.1 Sibling Rivalry in Mixed-Sex Broods . . . . . . . . . . . . . . 4.4.2 Dual Roles of Precocious Larvae in Competition . . . . . . 4.4.3 Aggression Toward Closer Relatives . . . . . . . . . . . . . . . 4.4.4 Kin Recognition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.4.5 Effects of Relatedness on the Brood Size and Sex Ratio in Copidosoma koehleri . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

103 110 111 111 112 116 119 133 133 134 136 138 142 142 143 145 146 147 148 148 150 151 152 152 154 156 157 157 158

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Ecology and Evolution of Polyembryony . . . . . . . . . . . . . . . . . . . . . 5.1 Evolutionary Development of Polyembryony . . . . . . . . . . . . . . 5.1.1 Environmental Conditions Favoring the Evolution of Polyembryony in Aquatic Invertebrates . . . . . . . . . . 5.1.2 Developmental Constraints Favoring the Evolution of Polyembryony in Armadillos . . . . . . . . . . . . . . . . . 5.1.3 Evolution of Polyembryony in Parasitic Insects . . . . . . 5.2 Eusociality in Polyembryonic Encyrtids . . . . . . . . . . . . . . . . . . 5.2.1 Eusociality in Polyembryonic Hymenoptera . . . . . . . . . 5.2.2 Evolution of the Soldier Caste in Copidosoma floridanum . . . . . . . . . . . . . . . . . . . . . . . 5.2.3 Evolution of the Soldier Caste in the Genus Copidosoma . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.3 Brood Size, Body Size, and Their Trade-Off . . . . . . . . . . . . . . . 5.4 Oviposition Behavior . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.4.1 Host Handling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.4.2 Oviposition of Male and Female Eggs . . . . . . . . . . . . . 5.5 Sex Allocation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.5.1 Sex Ratio in Mixed-Sex Broods of Polyembryonic Parasitoids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.5.2 Local Mate Competition (LMC) . . . . . . . . . . . . . . . . . 5.5.3 Effects of Host Density and Parental Density on Brood Size and Brood Sex Ratio . . . . . . . . . . . . . . . . . . . . . . 5.6 Mechanism for the Evolution of Polyembryonic Development in Insects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

. 163 . 164 . 165 . . . .

165 166 172 172

. 174 . . . . . .

175 175 178 178 178 179

. 179 . 181 . 183 . 183 . 186

Subject Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 193 Taxonomy Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 197

Chapter 1

Overview of Polyembryony

1.1

Definition of Polyembryony

Polyembryony is a unique form of asexual reproduction whereby multiple offspring are produced from a single egg or zygote. To use Craig et al.’s (1997) words, polyembryony is a paradoxical combination of two reproductive modes—sexual and asexual reproduction. Nevertheless, it has evolved and been maintained in a wide range of taxa, including rust fungi (Alexopoulos 1952; Craig et al. 1997), algae (Searles 1980), and animals (Craig et al. 1997; Sköld et al. 2009), including the wellknown phenomenon of identical twins in humans. The term “polyembryony” was first used in botany by Leeuwenhoek in 1719, who reported twin embryos in orange (Lakshmanan and Ambegaokar 1984), following which Strasburger (1878) demonstrated the phenomenon in several angiosperm genera. The term was subsequently introduced to zoology by Marchal (1898a, b), who applied it to the phenomenon that occurs in parasitic Hymenoptera. Since that time, the term “polyembryony” has been used in both botany and zoology. However, the meaning of the term differs between the two fields. In botany, “polyembryony” refers to the condition where a non-zygotic embryo that originated from cells other than the egg cell develops in the same seed as the zygotic embryo, whereas in zoology, it is applied to the situation where multiple individuals develop from a single zygote (Lakshmanan and Ambegaokar 1984). Narrowly defined, polyembryony refers to embryonic cloning, where fission of the cells produces separate embryos (Moore 1981; Bosch et al. 1989), while in broader terms, it also encompasses the production of individual, post-embryonic clones (Craig et al. 1997). In each case, the offspring that develop from the single zygote are genetically identical to each other but different from the parents. Various asexual, but not polyembryonic, modes of reproduction exist in the animal kingdom. For example, aphids switch between sexual and asexual modes of reproduction seasonally, with the latter involving the production of offspring by viviparous parthenogenesis from different unfertilized ova. In addition, some © Springer Nature Singapore Pte Ltd. 2019 K. Iwabuchi, Polyembryonic Insects, Entomology Monographs, https://doi.org/10.1007/978-981-15-0958-2_1

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1 Overview of Polyembryony

cnidarians (hydra) proliferate by budding, and others (sea anemones) undergo fragmentation, while poriferans (sponges) reproduce both sexually and asexually by budding, and turbellarians (flatworms) reproduce by fission, budding, and fragmentation. Since these reproductive modes are not based on the production of offspring from an egg, they should be considered as somatic colony formation, similar to vegetative propagation in plants. However, at the molecular level, parts of these reproductive modes do share common feature with polyembryony. For example, the long-term maintenance of totipotency, which is the ability to regenerate a whole new individual organism through the fission of cells and budding, as seen in primitive metazoans, may be advanced by the same molecules and mechanisms as are involved in polyembryony.

1.2

Category of Polyembryony

Marchal (1904) separated polyembryony into three categories: (1) experimental, (2) accidental (sporadic and teratological), and (3) specific (obligate, consistent, and constitutive). Experimental polyembryony refers to the case where polyembryony is induced by natural experiments or artificial manipulations (Huxley and Beer 1934; IvanovaKasas 1972). Polyembryony caused by natural experiments has been identified in killifish and trout when their eggs are subjected to harmful low temperatures or oxygen deficiency, while polyembryony caused by artificial manipulations, such as surgical splitting or shaking, has been observed in the camel cricket and amphioxus (Krause 1962). Accidental polyembryony applies to situations where polyembryony occurs at a low frequency. The most famous case is monozygotic twinning (identical twinning) in humans, which occurs at a frequency of 0.35% (Bulmer 1970; MacGillivray et al. 1975). Twinning has also been reported in other animals but is generally associated with high mortality. Accidental polyembryony is found in many taxa (Patterson 1927; Craig et al. 1997), e.g., turbellarians (Benazzi and Benazzi Lentati 1993), gastrotrichs (Hummon and Hummon 1993), Anthomedusae (Shostak 1993), and Chordata (Olsen 1962; Stansfie 1968; Kaufman 1982; Laale 1984; Ashworth et al. 1998). Accidental embryo twinning has also been described in many insects with short germ bands (Cappe de Baillon 1928; Slifer and Shulow 1947; Prevost and McFarlane 1979; Cabrero et al. 1996). All instances of accidental polyembryony represent maladaptations (Patterson 1927). However, monozygotic twinning in humans and in some cases other mammals may be a genetic and evolutionarily significant trait. Therefore, “occasional polyembryony” or “sporadic polyembryony” (Ivanova-Kasas 1972) may be more appropriate than “accidental polyembryony” in these instances. It should also be noted that Craig et al. (1997) argued that accidental polyembryony, together with parthenogenetic multiplication by juveniles and early coloniality, should not be considered a form of polyembryony.

1.3 Polyembryony in Animals

3

Specific polyembryony is a form of polyembryony that represents the normal manner of development and has been found in armadillos and parasitic insects, including one species of Strepsiptera and many species of Hymenoptera. This form of polyembryony is more commonly called “obligate polyembryony.” Facultative polyembryony refers to the situation where polyembryony occurs at the same time as monoembryony. For example, in the parasitoid wasp Platygaster hiemalis, the embryos can develop monoembryonically or as twins (Ivanova-Kasas 1972). In addition to the above, there are several other forms of polyembryony that are outside the definition. These include pseudo-polyembryony, which is the development of twin-like individuals from so-called complex eggs that originated from the fusion of two or more oocytes (Counce 1968; Ivanova-Kasas 1972), and substitutive polyembryony, which occurs when the initial embryo, after developing well, perishes and a new embryonic rudiment subsequently develops normally (Vignau 1967; Ivanova-Kasas 1972).

1.3

Polyembryony in Animals

The occurrence of polyembryony in the animal kingdom has been well reviewed by Craig et al. (1997), who listed the taxa that contain polyembryonic species with their life habits and discerned the evolution of this mode of reproduction. Polyembryony is distributed across six phyla, from the primitive metazoans to mammals [Cnidaria, Bryozoa (Ectoprocta), Platyhelminthes, Echinodermata, Chordata, and Arthropoda, Table 1.1]. Polyembryony that occurs at the post-embryonic or larval stages of aquatic invertebrates remains controversial because it is not obligatory but rather is Table 1.1 Polyembryony in the animal kingdom Phylum Cnidaria

Class Hydrozoa

Subclass/order Trachylina Hydroida

Bryozoa (Ectoprocta)

Stenolaemata

Cyclostomata

Platyhelminthes

Trematoda Monogenea Cestoidea Asteroidea Ophiuroidea Mammalia Crustacea Insecta

Digenea Gyrodactyloidea Eucestoda Paxillosida Ophiurida Edentata Rhizocephala Hymenoptera Strepsiptera

Echinodermata Chordata Arthropoda

References Shostak (1993) Shostak (1993), Bigelow (1909), Berrill (1949) Borg (1926, 1933), Calvet (1900), Harmer (1890, 1893) Noble et al. (1989) Kathariner (1904) Noble et al. (1989) Jaeckle (1994), Bosch et al. (1989) Mortensen (1921) Galbreath (1985) Glenner and Høeg (1995) Strand (1989), Godfray (1994) Jeannel (1951)

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1 Overview of Polyembryony

often facultative. Moreover, there is the basic question of whether cloning that occurs at such late developmental stages represents polyembryony at an extended phase of embryogenesis or asexual propagation of the growing organisms. However, larval cloning often occurs frequently in aquatic invertebrates and, in most cases, is part of the regular reproductive system. Most polyembryonic species have a parasitic, in particular endoparasitic, lifestyle.

1.3.1

Cnidaria

The phylum Cnidaria includes four classes: Scyphozoa (jellyfishes), Anthozoa (sea anemones and corals), Cubozoa (box jellyfishes), and Hydrozoa (hydrozoans). The life cycle of Cnidaria has two distinctive stages: (1) formation of the planula (larval form) and its transformation to the polyp and (2) formation of the medusa from the polyp tissues. The life cycle of sexually reproducing Cnidaria involves both sessile polyp and swimming medusa stages. In freshwater hydrozoans, the fertilized egg first attaches itself to the parental polyp, following which the embryo later detaches and the planula hatches. In the marine hydrozoan Podocoryne carnea, the swimming larva, which is known as a planula and originated from a fertilized egg, anchors itself to the substrate to form a primary polyp. This primary polyp can then produce additional polyps asexually by budding or stolonic outgrowth to form a clone or a colony. The early medusa of P. carnea is formed by dedifferentiation of the polyp cells, which proliferate intensively (Brändli 1971; Bölsterli 1977). Hydrozoans in the order Narcomedusae also include both sexual and polyembryonic modes of reproduction in their life cycle (Craig et al. 1997). In the marine hydrozoan Pegantha smaragdina, the larva buds within the parent through polyembryony and then liberates medusae, while the marine species Cunina proboscidea produces adult female medusae from an unfertilized egg via a complex asexual process that involves polyembryonic budding and apomixis (Craig et al. 1997). In the freshwater hydrozoan Polypodium hydriforme, which is an endoparasite of the European starlet (Sturnus vulgaris) and sturgeon, the morula and larva are enveloped by the trophamnion, which is derived from the second polar body, and develop inside the oocyte of the host (Raikova 1980). In this species, the free-living stages correspond to the medusae in other narcomedusan hydrozoans and the endoparasitic stages correspond to the polyps (Bouillon 1985). Each larva, which is a two-layered planula measuring approximately 1 mm, develops into a colony with a stolon and dozens of buds. Polyembryony occurs in this organism when the stolon splits apart and each undergoes fission (Raikova 2008) (Fig. 1.1a, b). Polyembryony has also been reported in jellyfishes, in which the polyp splits horizontally into disks that become free-swimming medusae. Thus, polyembryony in a broad sense is thought to be a regular reproduction mode in Cnidaria (Galliot and Schmid 2002).

1.3 Polyembryony in Animals

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Fig. 1.1 Cnidaria. (a) Life cycle of Polypodium hydriforme. (A) Stolon with internal tentacles inside the egg before spawning; (B) stolon with external tentacles emerging from an egg at the time of spawning; (C) free stolon in water; (D) fragment of a stolon; (E) 12-tentacled specimen; (F) 24tentacled specimen; (G) 6-tentacled specimen; (H) 24-tentacled specimen with 4 “female” sexual complexes; (I) 12-tentacled specimen with 4 “male” gonads; (J) binuclear parasitic cell; (K) morula encircled by a trophamnion; (L) planula; (M) budding planula; (N) stolon without tentacles; (O) stolon with internal tentacles. (b) Magnification of free-living stages: everted stolon and longitudinal fission. (A) Everted stolon, (B) Fragment of a stolon and (C) Fission. (Raikova 2008)

1.3.2

Bryozoa (Ectoprocta)

Bryozoans, or moss animals, are hermaphroditic, aquatic invertebrates that live in colonies of interconnected, small (